Detection of Methicillin Resistant Staphylococcus aureus Isolated from Human and Animals in Basra Province / Iraq

Abstract

During the period from October 2010 to March 2011, two hundred eighty five specimens were collected from AL-Basra province and surveyed for the occurrence of methicillin resistant Staphylococcus aureus (MRSA). Depending on the source of collection, specimen were divided into 6 groups (124 samples of cow milk, 25 samples of cow nasal swabs, 56 samples of sheep nasal swabs, 20 samples of goat nasal swabs, 33 samples of human nasal swabs (obtained from nosocomial infection) and 27 samples of environmental swabs). A total of 72 samples was positive for S. aureus were identified: 35/72 (48.61%) isolates from cow milk, 1/72 (1.38%) isolate from cow nasal swabs, 7/72(9.72%) isolates from sheep nasal swabs, 1/72 (1.38%) isolate from goat nasal swabs, 19/72(26.38%) isolates from human nasal swabs and 9/72(12.5%) isolates from environmental swabs, depending on morphological, cultural, microscopical characterization and biochemical tests. Susceptibility of 72 S. aureus isolates to 18 different antibiotics. The present study aims to investigate the presence of methicillin resistant Staphylococcus aureus in animals and human samples.

Full text

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Mirror of Research in Veterinary Sciences and Animals (MRVSA)
Original Article
Detection of Methicillin Resistant Staphylococcus aureus Isolated from Human
and Animals in Basrah Province / Iraq
Bassam Y. Khudaier
1
, Basil A. Abbas
1
*, Amaal M. Khudaier
1
College of Veterinary Medicine , University of Basra, Iraq
*Corresponding author: Dr. Basil A. Abbas
Email: basilabbas63@yahoo.com
Abstract
During the period from October 2010 to March 2011, two hundred eighty five
specimens were collected from AL-Basra province and surveyed for the occurrence of
methicillin resistant Staphylococcus aureus (MRSA). Depending on the source of
collection, specimen were divided into 6 groups (124 samples of cow milk, 25 samples
of cow nasal swabs, 56 samples of sheep nasal swabs, 20 samples of goat nasal swabs,
33 samples of human nasal swabs (obtained from nosocomial infection) and 27
samples of environmental swabs). A total of 72 samples was positive for S. aureus were
identified: 35/72 (48.61%) isolates from cow milk, 1/72 (1.38%) isolate from cow nasal
swabs, 7/72(9.72%) isolates from sheep nasal swabs, 1/72 (1.38%) isolate from goat
nasal swabs, 19/72(26.38%) isolates from human nasal swabs and 9/72(12.5%) isolates
from environmental swabs, depending on morphological, cultural, microscopical
characterization and biochemical tests. Susceptibility of 72 S. aureus isolates to 18
different antibiotics. The present study aims to investigate the presence of methicillin
resistant Staphylococcus aureus in animals and human samples.
Keyword: Methicillin, Staphylococcus aureus, MRSA, human, cow, sheep.
To cite this article: Bassam, Y. Khudaier; Basil, A. Abbas; Amaal M. Khudaier.2013.
Detection of Methicillin Resistant Staphylococcus aureus Isolated from Human and
Animals in Basrah Province / Iraq. Mirror of Research in Veterinary Sciences and
animals. MRSVA 2 (3), 12-21.
Introduction
Staphylococcus aureus is bacterium found passively colonizing skin and nasal
passages of healthy humans and animals (Rohde, 2011), though this opportunistic
pathogen colonizes without causing disease(Davis et al., 2004).

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Nasal carries of S. aureus bear an increased risk to become septic, once bacteria
gain access to the bloodstream due to breaches in the nasopharyngeal or other mucosal
colonized niches (Wertheim et al., 2004; Wertheim et al., 2005). The association of
owners and veterinarian staff with human healthcare sector (HCS) and animal –related
characteristics such as signalment, antimicrobial, immunosuppressive therapy and
surgery were evaluated as putative risk factors using logistic regression (Magalhaes et
al., 2010).
Methicillin–resistant Staphylococcus aureus (MRSA) has become important
acquired pathogen in hospital and also livestock (LA-MRSA) in recent years. MRSA
associated with (LA-MRSA) have been reported worldwide in many species (Persoons
et al., 2009; de Neeling et al., 2007; Smith et al., 2008). MRSA produce a low affinity
penicillin binding protein (PBP2 orPBP2a) in addition to the usual PBPs (Hartman and
Tomasz, 1984). Furthermore, MRSA strains are resistant to gentamicin, kanamycin,
tobramycin, microldes, tetracycline and fluoroquinolones. Thus, multiple resistance of
S. aureus strains occur (Chambers et al., 1997; Petinaki et al., 2001; Maddox, 2011).
For humans, S. aureus are important causes of food poisoning,
pneumonia,wound infection and nosocomial bacteremia (Horan et al.,1988). S. aureus
also expresses certain virulence factors and due to these virulent determinants, it is
tenacious, potentially destructive and shows increasing resistance to antimicrobial
agents (Burriel, 1998).
Staphylococcus spp. causes severe disease such as mastitis (Hassan and Yousif
2013) , arthritis and urinary tract infection by introducing numerous virulence factors
such as extracellular toxins and enzymes into animal species (Waldvogel, 1990). This
study intends to detect the methicillin resistant Staphylococcus aureus isolated from
human and animals in Basrah Province / Iraq .
Materials and Methods
Samples collection
Two hundred eighty- five samples were collected from animals, human and
environment during the period from October, 2010 to March, 2011 from Basra villages.
One hundred and twenty four milk samples were collected from cow with clinical
mastitis and normal milk cow, 25 cow nasal swabs, 56 sheep nasal swabs and 20 goat
nasal swabs. Thirty three samples were collected from human nasal swabs from AL-
Basra General hospital in Basra city. Twenty seven samples were collected from open
area of AL-Basra General hospital in Basra city.
Laboratory diagnosis
The specimens were directly inoculated onto mannitol salt agar (MSA) and
incubated at 37 ºC for 24 hrs. All colonies from primary cultures were purified by
subculture onto MSA medium and incubated at 37ºC for 24- 48 hrs. (Talan et al., 1989(.
Gram stain were investigated according to Barrow and Feltham (2003).
Biochemical tests

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Free coagulase Test : One ml of 18 hrs culture broth was added to 0.1 ml of human
plasma without dilution and incubated at 37 ºC for 4 hrs. the clotting hourly noticed.
The appearance of the clotting indicates a positive result comparable to control
(Macfaddin, 2000).
Catalase Test: A small amount of pure growth was transferred with a wooden stick
from MSA into clean slide, then a drop of catalase reagent was added. The evolution of
gas bubbles indicates a positive result (Macfaddin, 2000).
Oxidase Test: A filter paper was moistened with several drops of oxidase reagent 1%
then a small portion of the colony was removed with a sterile wooden stick rabbed on
moistened filter paper. A positive reaction is indicated by the appearance of dark or
deep purple color within 10-20 sec. (Macfaddin, 2000).
Nitrophenl-B-D-galactopyranoside (ONPG): Small portion from the colony was
mixed with 1 ml of D.W in sterile tube and homogenized then a disc of ONPG was
added. The incubation took place at 37 ºC and the results were read after 1- 4-24 hrs.
The colourless and yellow color indicates negative and positive results, respectivily
(Macfaddin, 2000).
DNase Production Test: Over-night incubated of bacterial isolates were streaked on
DNase agar and incubated at 35 ºC for 24hrs. The bacterial growth was flooded with 1N
hydrochloric acid (HCl). The appearance of clear zone around of the colonies indicates
positive result (MacFaddin, 2000).
Antibiotics susceptibility test
The antibiotic susceptibility testing was done by the agar discs diffusion method
as described by Kirby and Bauer, (1966). Three isolated colonies of the same
morphological type were selected from the agar plat culture. The top of each colony was
touched with a loop and the growth was transferred into a tube containing 5 ml brain
heart infusion (BHI) and incubated at 35 ºC for 48 hrs.. The turbidity of the actively
growing broth culture was adjusted to the 0.5 McFarland standard.
Fifteen minutes post the adjustment sterile cotton swab was dipped into adjusted
suspension, then rotated several times and pressed firmly on the side of the tube above
the fluid level. The dried surface of the a Mueller–Hinton agar (MHA) plate was
inoculated by streaking the swab over the entire sterile agar surface .This procedure was
repeated by streaking two more times, rotating the plate approximately 60° each time to
ensure an even distribution of the inoculums. The predetermined antimicrobial disks
were dispensed on to the surface of the inoculated agar plate. Each disk was pressed
down individually to ensure complete contact with agar surface.
The plates were inocubated for 18hrs. at 35 ºC. The resulting zone of inhibition was
uniformly circular with confluent lawn of growth. The diameters of the zones of
complete inhibition were measured, including diameter of the disk. The size of
inhibition zones were interpreted by referring to zone diameter interpretive standard
from Bioanalyse sensitivity discs Ankara/Turkey
Results
Isolation and Identification of Saphylococcus aureus

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Cultural and biochemical examination of 285 samples revealed isolation of 72 S.
aureus strains. The highest rate of S. aureus isolates was observed in human nasal
swab19/33(57.57%) followed by environmental swab 9/27(33.33%), cow milk
35/124(28.22%), then sheep nasal swab7/56(12.5%), while goat nasal swab and cow
nasal swab where found to have the lowest rate 5% and 4% respectively, with
significant differences (P< 0.05) in the rate of S.aureus isolation among the different
samples as showed in table 1.
The present study revealed that (90.90%) of staphylococcal isolates from human
nasal samples were positive to coagulase test followed by environmental swabs
(81.48%), cow nasal swabs and goat nasal swabs (80 %), sheep nasal swabs (75%) and
while cow milk (65.32%). There were no significant differences (p>0.05) between
numbers of isolates in different samples.
DNase test revealed that the highest percentage was showed in human nasal
swabs were (75.75%), followed by environmental swabs (70.37%), cow milk (33.87%),
sheep nasal swabs (26.78%), goat nasal swabs (25%) and cow nasal swabs (24%). There
were significant differences (P < 0.05) between numbers of isolates in different
samples.
Table (1): Number and percentage of S. aureus isolated from different sources
In ONPG test the highest percentage in staphylococcal human nasal samples were
(57.57%), followed by environmental swabs, cow milk, sheep nasal swabs which were
(33.33%), (28.22%), (12.5%) respectively, while the lowest percentage observed in
goat nasal swabs and cow nasal swabs were (5%and 4%) respectively. There were
significant differences (p<0.05) between numbers of isolates in samples.
All staphylococcal isolates from different sources showed catalase positive and
oxidase negative (Table 2).
Screening for Methicillin (Oxacillin) Resistance S. aureus
By using disc diffusion method, 72 S. aureus isolates were tested for
susceptibility toward oxacillin (table 3). Total of 25(34.72%) of S. aureus were MRSA
which were isolated from this study. The highest percentage of methicillin resistance
was in human nasal swabs (42.1%), followed by cow milk (40%) then environmental
swabs (33.33%). While sheep nasal swabs, goat nasal swabs and cow nasal swabs were
sensitive to methicillin. There were no significant differences (P > 0.05) in the
percentage of MRSA was isolated from different samples.
Type of samples
No. of samples
No. S. Aureus
(%)
Cow milk
124
35
(28.22)
Cow nasal swab
25
1
(4)
Sheep nasal swab
56
7
(12.5)
Goat nasal swab
20
1
(5)
Human nasal swab
33
19
(57.57)
Environmental swab
27
9
(33.33)
Total
285
72
(25.26)
X
2
= 90.563 (p<0.05)

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Table (2) Biochemical test of Staphylococcus aureus isolates from different sources
Test
Samples
Coagulas +
No.
(%)
DNase +
No.
(%)
ONPG –
No.
(%)
Catalase +
No.
(%)
Oxidase-
No.
(%)
Cow milk
81/124
(65.32)
42/124
(33.87)
35/124
(28.22)
124/124
(100)
124/124
(100)
Cow nasal swab
20/25
(80)
6/25
(24)
1/25
(4)
25/25
(100)
25/25
(100)
Sheep nasal swab
42/56
(75)
15/56
(26.78)
7/56
(12.5)
56/56
(100)
56/56
(100)
Goat nasal swab
16/20
(80)
5/20
(25)
1/20
(5)
20/20
(100)
20/20
(100)
Human nasal swab
30/33
(90.90)
25/33
(75.75)
19/33
(57.57)
33/33
(100)
33/33
(100)
Environmental swab
22/27
(81.84)
19/27
(70.37)
9/27
(33.33)
27/27
(100)
27/27
(100)
Average (%)
(78.84)
(42.62)
(23.43)
(100)
(100)
X
2
4.653
(P>0.05)
66.547
(P<0.05)
90.78
(P<0.05)
0
0
Table (3) Susceptibility of S.aureus isolates to the methicillin (oxacillin)
Samples
No. of strains
No.MRSA
strains (%)
No.MSSA
strains (%)
Cow milk
35
14(40)
21(60)
Cow nasal swab
1
0(0)
1(100)
Sheep nasal swab
7
0(0)
7(100)
Goat nasal swab
1
0(0)
1(100)
Human nasal swab
19
8(42.1)
11(57.9)
Environmental swab
9
3(33.33)
6(66.66)
Total
72
25(34.72)
47(65.28)
X
2
1.165(P>0.05)
27.821(P<0.05)

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Antibiotic susceptibility testing of S. aureus isolates
Figure (1) summarise the percentage of susceptibility results of 18 different
antibiotics by disc diffusion test against 72 S. aureus. The susceptibility to ceftriaxone
was (100%), to cefotaxime (90.27%), to ampecillin (61.11%), vancomycin (59.72%),
carbencillin (56.94%), oxacillin (34.72%), lincomycin (38.88%), pencillin (33.33%),
The less susceptible results were showed to gentamycin (23.61%), erythromycin
(15.27%), doxycillin (11.11%), tecoplanine (9.72%), clindamycin (8.33%),
ciprofloxacin (6.94%) and nitrofurantoin, chloramphenicol, tobramycin and
azithromycin (0%).There were significant differences (P<0.05) of S. aureus isolates
between different types of antibiotics.
Figure (1). The percentage of antibiotics susceptibility of S. aureus isolates.
Ceftriaxone(CRO), azithromycin(AZM), tobramycin(TOB), chloramphinicol(C),
nitrofurantion(F), carbencillin(PY), ciprofioxacin(CIP), cefotaxime(CTX),
doxycillin(DO), erythromycin(E), lincomycin(L), gentamycine(CN), clindamycin(DA),
penicillin(P), ampecillin(AM), tecoplanin(TEC), vancomycin(VA),
oxacillin(OX).
Discussion
Staphylococcus aureus is one of the most commonly identified
pathogens in human
medicine and is the major cause infections of nosocomial
and animals (Boyce et al.,
1983; Rohde, 2011) and community-acquired infections
(Naimi., et al., 2003; Said-
Salim et al., 2003). The present study agreed with a number of studies dealing with
human, AL- Saady, (2007), who isolated S. aureus from different samples of human in

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percentage of (66.7%). Abbas (1989) isolated S. aureus from healthy nutrition workers
(carriers) in the Hospital of Medical City of Baghdad, the percentage of S. aureus
isolated from nasal swab range between 18-34%, from hand, 29-55%, from throat swab,
9-18%, while the higher percentage was isolated from old workers, 62-80%. The
percentage of S.aureus isolated from human in different samples appeared 32.6% at the
study of (Saleh, 1990). The causes of this distribution of S. aureus in different hosts is
due to number of virulence factors which help to colonize, invade and infect different
hosts. The present study showed that S. aureus are present in human nasal swabs
57.57%, environmental swabs 33.33% and cow milk 28.22%, when compared to other
sources, they form low levels isolations. These results are in line with Hanon (2009),
who reported that S. aureus was isolated from bovine milk, 48.57% and nasal swab,
52.85%, while the isolation percentage from human was 59.83%, stool 55.2%, urine
86.06% and nasal swab 63.33%.
Seventy two S. aureus isolates were tested against various antibiotics. The results
showed that beta-lactam antibiotic (oxacillin), showed percentage of susceptibility
65.28%. This result is agreement to the study of Hanon (2009), who mentioned that the
percentage of susceptibility of oxacillin was 52.5%. It is also similar to the findings that
were found in the study of Omer (2010) who detected the MRSA in a percentage of
(50%) from the buffalo milk. Compared with the present study, low percentage of
MRSA were detected in bovine milk by Idbeis (2010), Farzana et al., (2004) and
Devriese et al.(1997),whom recorded percentage of MRSA were 10.52%, 10%, and
10% respectively.
In the present study, susceptibility of S. aureus isolates to vancomycin was
40.28%. Similar finding were obtained in the study of Hanon (2009) who recorded that
55% of S. aureus isolates from bovine were sensitive to vancomycin. On the other hand,
all S. aureus isolates were 100% sensitive to vancomycin (Falcao et al., 1999; Santos et
al., 1999; Panhotra et al., 2005; Bendahou et al., 2008; AL- Khudheiri, 2008; Idbeis,
2010). AL-Saady (2007) mentioned that S. aureus isolated from human in different
samples revealed complete resistance to vancomycin.
The antibiotic sensitivity testing reveals that S. aureus isolates were sensitive
100% to antibiotics like nitrofurantion, chloramphinicol, tobramycin, and azithromycin
for each one. These results are in line with the study of Panhotra et al., (2005), who
mentioned that the sensitivity to chloramphinicol was 100%. These results are also in
agreement with Bendahou et al., (2008), who reported that S. aureus isolates from raw
milk and milk product appeared to be sensitive to tobramycin 95%, nitrofurantion
100%, chloramphinicol 95%. AL-Khudheiri (2008), and Santos et al., (1999), stated
that S. aureus isolates were resistant to chloramphinicol 58.4% and 85%, respectively.
The sensitivity of S. aureus isolates to gentamycin was 76.39%. A similar
finding was obtained by the study of AL-Marsomy (2008), who recorded sensitivity of
S aureus isolates from mastitis togentamycin was 76.8%, but the highest sensitivity
(100%) was found by the study of (Ismaiel, 1986; Abd-AL-Rahman, 1989 and
Bendahou et al., 2008).
Staphylococcus. aureus isolates from different sources showed 84.73%
susceptibility to erythromycin. This result is in agreement with the study of
Ismaiel,(1986), who mentioned that 89% of S. aureus being isolated from bovine to
have appeared sensitivity to erythromycin. Bendahou et al., (2008), on the other hand
revealed that S. aureus being isolated from raw milk and milk product represented high

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susceptibility (90%) to erythromycin. Also Hanon, (2009), reported that sensitivity of S.
aureus to isolated from human and animals to erythromycine were 25% and 37.5%
respectively.
In the present study, S. aureus isolates were (38.88%) and (8.33%) resistant to
lincomycin and clindamycin, respectivily. These results agree with the study of Bratu et
al.(2005), who found the resistant of S. aureus isolated from hospital nursery and
maternity units to to lincomycin and clindamycin during 1999, 2001 and 2003, were
18%, 15% and 20%, respectively. Hanon, (2009), mentioned that the sensitivity of S.
aureus to erythromycine was(52.5%) in bovine, but it was (70%) in human. Finally we
conclude that the samples collectd from human or animal can be contaminated with
drug resistance S. aureus wich involved in serious health problems.
References
Abbas, M. R. (1989). Contamination of environment and nutrition by Staphylococcus
aureus in hospital of medical city and AL – Kandy. M.Sc., Thesis, College of
Veterinary Medicine, University of Baghdad. (In Arabic).
Abd-AL- Rahman, A. M. (1989). Staphylococcus aureus isolation from camel. M. Sc.,
Thesis, College of Veterinary Medicine, University of Bagdad. (In Arabic)
AL-Khudeiri, M. K. (2008). Bacteriological and genetic study of methicillin resistant
Staphylococcus aureus isolated from the hospitals of Najaf City. M.Sc., Thesis, College
of Education for Girls. University of Kufa. (In Arabic)
AL-Marsomy, H. M. (2008). Isolation and diagnostic some causative bacterial, causes
of mastitis in cows and role lactobacillus secretion at inhibition growth of
Staphylococcus aureus. M.Sc., Thesis, College of Veterinary Medicine, University of
Baghdad. (In Arabic)
AL-Saady, A. A. (2007). Extraction and characterization of surface adherence protein
from methicillin resistance Staphylococcus aureus and study of the pathogenic effects.
Ph.D., Thesis, College of Science, University of Baghdad. (In Arabic)
Barrow and Feltham (2003). Cowan and Steelʼs. Manual for the identification of
medical bacteria. 2
nd
Ed. Cambridge University press Cambridge, London, New
York.USA.
Boyce, J. M.; White, R. L. and Spruill, E. Y. (1983). Impact of methicillin-resistant
Staphylococcus aureus on the incidence of nosocomial staphylococcal infections. J
.Infect. Dis. 148: 763.
Bratu, S.; Eramo, A.; Kopec, R.; Coughlin, E.; Ghitan, M.; and Yost, R.,
Chapnick EK, Landman D, Quale J. (2005). Community associated methicillin-
resistant Staphylococcus aureus in hospital nursery and maternity units. Emerg Infect
Dis. 11(6):808-813.
Burriel A.R. (1998). Isolation of Coagulase positive staphylococci from the milk and
environment of sheep. J. Dairy Sci. 65: 139-142.
Chambers, H. F. (1997). Methicillin resistance staphylococci; molecular and
biochemical basis clinical implications. Clin. Microbiol. Rev. 781-791.
Davis, K. A.; Stewart, J. J.; Crouch, H. K.; Florez, C. E. and Hospenthal, D. R.
(2004). Methicillin-resistant Staphylococcus aureus (MRSA) nares colonization at
hospital admission and its effect on subsequent MRSA infection. Clin. Infect. Dis. 39:
776-782.

MRVSA 2(3), 12-21. Khudaier, et al, 2013
http://mirrorofresearchinveterinarysciencesandanimals.com/
8073-ISSN 2307

Devriese, L. ; Haesebrouck, F. ; Hommez, H. and Vandermeersch, R. (1997). A 25-
year survey of antibiotic susceptibility testing in Staphylococcus aureus from bovine
mastitis in Belgium, with special reference to penicillinase”, J. Vlaams
Diergeneeskundig Tijdschrift. 66: 170-173.
Falcao, M. H. L.; Texeira, L. A.; Ferreira, B. T.; Borgeges, A. A.; and Figueiredo,
A. M. S. (1999). Occurrence of methicillin-resistant and susceptible Staphylococcus
aureus within a single colony contributing to methicillin-resistant S. aureus mis-
identification. J. Med. Microbiol. 48: 515-521.
Farzana, K. ; Shah, S. and Jabeen, F. (2004). Antibiotic resistance pattern against
various isolates of Staphylococcus aureus from raw milk samples. J. Res. Sci. 15:145-
151.
Hanon, B. M. (2009). Comparative study to the Staphylococcus aureus, isolated from
the bovine and human with detection of virulence (coa) gene in these isolates by
polymerase chain reaction. M.Sc. Thesis, College of Veterinary Medicine, University of
Basrah.
Hartman, B. J. and Tomasz, A. (1984). Low-affinity penicillin-binding protein
associated with β-lactam resistance in Staphylococcus aureus. J. Bacteriol. 158:513-
516.
Horan, T.; Culver, D. and Jarvis, W. (1988). Pathogens causing nosocomial
infection: preliminary data from the national nosocomial infections surveillance system.
Antimicrob. Newsl. 5:65-67.
Idbies, H. I. (2010). Detection of enterotoxin genes (sea-see) of Staphylococcus aureus
isolated from raw milk by multiplex PCR and study of their pathogenicity. M.Sc.
Thesis, College of Veterinary Medicine. University of Basrah.
Ismaiel, B. M. (1986). Systems for phage typing of Staphylococcus aureus of animal
origin. M.Sc. Thesis, College of Veterinary Medicine, University of Bagdad. (In
Arabic)
Kirby, W. M. and Bauer, A. W. (1966). Antibiotic susceptibility testing by a
standardized single disc method .The American. J. Clin. Path. 45 :493-496.
Macfaddin, J. F. (2000). Biochemical tests for identification of medical bacteria. 3
rd
Ed. Lippincott Williams and Wilkins USA.
Maddox, C. W. (2011). Transfer of methicillin resistance and virulence factors between
staphylococci. AAVLD Bacteriology/Mycology Sub-committee Mini-Symposium.
Sponsorship generously provided by: Biolog. Inc. and Pfizer Animal Health. New York,
USA.
Magalhaes, R. S.; Loeffler, A.; Lindsay, J.; Rich, M.; Roberts, L.; Simth, H.;
Lloyd, D.H. and Pfeiffer, D. U. (2010). Risk factors for methicillin-resistant
Staphylococcus aureus (MRSA) infection isolated in dogs and cats: a case-control
study. J. Vet. Res. 41: 55.
Mustafa Salah Hassan and Afaf AbdulrahmanYousif.(2013). Alteration of some
enzymatic activities in whey of ewe’s milk Suffered from Staphylococcal mastitis
Mirror of Research in Veterinary Sciences and animals. MRSVA 2 (2), 8-15.
Naimi, T. S.; LeDell, K. H.; Como-Sabetti, K.; et al., (2003). Comparison of
community- and health care-associated methicillin-resistant Staphylococcus aureus
infection. JAMA 290: 2976–2984.
Omer, H.S. (2010). Isolation of Staphylococcus aureus from ruminant’s milk and their
resistance to antibiotics in Ninevah governorate. Iraqi. J. Vet.Sci.24: 109-114.

MRVSA 2(3), 12-21. Khudaier, et al, 2013
http://mirrorofresearchinveterinarysciencesandanimals.com/
8073-ISSN 2307

Panhotra, B. R.; Saxena, A. K.; and Al-Mulhim, A. S. (2005). Chloramphenicol
susceptible methicillin-resistant Staphylococcus aureus in Eastern region of Saudi
Arabia. J. Saudi. Med. 26 : 1149-1151.
Persoons, D.; van Hoorebeke, S.; Hermans, K.; Butaye, P.; de Kruif, A.;
Haesebrouck, F.; et al. (2009). Methicillin-resistant Staphylococcus aureus in poultry.
Emerg. Infect. Dis. 15:452-453.
Petinaki, E.; Miriagou, V.; Tzouvelekis, Ls.; Pounaras, S.; Hatzi, F.; Kontos, F.;
Maniati, M. and Maniatis, A. N. (2001). Bacterial Resistance Study Group of
Thessaly. International Journal of Antimicrobial Agents. 18: 61-65.
Rohde, R. E. (2011). Methiillin-resistant Staphylococcus aureus (MRSA): A review of
the animal-human intersection. Methicillin- resistant staphylococci. AAVLD
Bacteriology/Mycology Sub-committee Mini-Symposium. Sponsorship generously
provided by: Biolog, Inc. and Pfizer Animal Health. New York, USA.
Said-Salim, B.; Mathema, B. and Kreiswirth, B. N. (2003). Community-acquired
methicillin-resistant Staphylococcus aureus: an emerging pathogen. Infect Control
Hosp. Epidemiol. 24: 451–455.
Saleh, A. H. (1990). Some side Staphylococcus aureus isolation from human and
different animals. M Sc. Thesis, College of Veterinary Medicine, University of Bagdad.
(In Arabic)
Santos, K. R. N.; Teixera, L. M.; Leal, G. S.; Fonseca, L. S. and Filho, P. P. G.
(1999). DNA typing of methicillin-resistant Staphylococcus aureus: isolates and factors
associated with nosocomial acquisition in two Brazilian university hospitals. Med.
Microbiol. 48: 17-23.
Smith, T. C; Male, M. J.; Harper, A. L.; Kroeger, J. S.; Tinkler, G. P.; Moritz, E.
D.; et al. (2008). Methicillin-resistant Staphylococcus aureus strain ST398 is present in
Midwestern U.S. swine and swine workers. PLoS One. 4:4258.
Talan, D. A. ; Staatz, D. ; Staatz, A. ; Goldstein, E. J. C. ; Singer, K. and Ocrturf,
G. D. (1989). Staphylococcus intermidius in canine gingival and canine-infected human
wound infections: Laboratory characterization of newly recognized zoonotic pathogen.
J. Clin. Microbiol. 27:78-81.
Waldvogel, F. A. (1990). Staphylococcus aureus, In Mandell, G.L.; Douglas, R. G. and
Bennett, J. E. (ed.), Principles and practices of infectious disease, 3
rd
ed. Churchill
Livingstone, New York, N.Y. Pp: 1489-1510.
Wertheim, H. F.; Melles, D. C.; Vos, M. C.; van Leeuwen, W.; van Belkum, A.;
Verbrugh, H. A. and Nouwen, J. L. (2005). The role of nasal carriage in
Staphylococcus aureus infections. Lancet. Infect. Dis. 5:751-762.
Wertheim, H. F.; Vos, M. C.; Ott, A.; van Belkum, A.; Voss, A.; Kluytmans, J. A.;
van Keulen, P. H.; Vandenbroucke-Grauls, C. M. ; Meester, M. H. and Verbrugh,
H. A. (2004). Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in
nasal carriers versus non-carriers. Lancet. 364:703-705.